Autocrine regulation of stomatal differentiation potential by EPF1 and ERECTA-LIKE1 ligand-receptor signaling

Xingyun Qi,Alex K Hofstetter,Masaki Ito,Soon-Ki Han,Keiko U Torii,Jacqueline M Garrick,Jonathan H Dang

doi:10.7554/elife.24102

Xingyun Qi, Alex K Hofstetter + Show 5 more

Open Access

https://doi.org/10.7554/elife.24102

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Abstract

Development of stomata, valves on the plant epidermis for optimal gas exchange and water control, is fine-tuned by multiple signaling peptides with unique, overlapping, or antagonistic activities. EPIDERMAL PATTERNING FACTOR1 (EPF1) is a founding member of the secreted peptide ligands enforcing stomatal patterning. Yet, its exact role remains unclear. Here, we report that EPF1 and its primary receptor ERECTA-LIKE1 (ERL1) target MUTE, a transcription factor specifying the proliferation-to-differentiation switch within the stomatal cell lineages. In turn, MUTE directly induces ERL1. The absolute co-expression of ERL1 and MUTE, with the co-presence of EPF1, triggers autocrine inhibition of stomatal fate. During normal stomatal development, this autocrine inhibition prevents extra symmetric divisions of stomatal precursors likely owing to excessive MUTE activity. Our study reveals the unexpected role of self-inhibition as a mechanism for ensuring proper stomatal development and suggests an intricate signal buffering mechanism underlying plant tissue patterning.

Highlights

Developmental patterning of multicellular organisms relies on positional cues as well as local cell-cell interactions
To clarify the role of EPIDERMAL PATTERNING FACTOR1 (EPF1)-ERL1 signaling during stomatal development, we first examined the in vivo dynamics of ERL1-YFP fusion protein driven by its promoter expressed in erl1-2 null mutant background (ERL1pro::ERL1-YFP in erl1)
ERL1-YFP signals were detected in the plasma membrane of both the meristemoid and neighboring stomatal lineage ground cell (SLGC) (Figure 1E,G,N; Video 1)

Summary

Introduction

Developmental patterning of multicellular organisms relies on positional cues as well as local cell-cell interactions. The GMC executes a single round of symmetric division to form paired guard cells (GCs) surrounding a pore, thereby completing stomatal differentiation (Lau and Bergmann, 2012; Pillitteri and Torii, 2012; Han and Torii, 2016) These cell state transitions are directed by the sequential actions of three basic-helix-loop-helix (bHLH) proteins, SPEECHLESS (SPCH), MUTE, and FAMA, which determine the initiation and proliferation, meristemoid-toGMC transition, and GMC-to-GC differentiation, respectively. These three bHLH proteins form heterodimers with the broadly expressed sister bHLH proteins SCREAM (SCRM: known as ICE1) and SCRM2, both of which are absolutely required for the activities of SPCH-MUTE-FAMA (Lau and Bergmann, 2012; Pillitteri and Dong, 2013; Han and Torii, 2016)

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